CRB-AAB MAY 18, David F. Albertini,Ph.D. Director of Laboratories, Senior Scientist Center For Human Reproduction
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1 Origin, mechanisms, and clinical consequences of embryo mosicism in humans" CRB-AAB MAY 18, 2017 David F. Albertini,Ph.D. Director of Laboratories, Senior Scientist Center For Human Reproduction
2 Conflict Statement Dr. Albertini Receives income from Springer/Nature Publishing, Inc. Has stock options in OvaScience, Inc. Is a member of the EMD Serono speaker bureau
3 Outline Origins of chromosomal and non-chromosomal mosaicism are gametic and zygotic Mechanisms of mosaicism involve perturbations in coordination between cell cycle, cytoskeleton, and chromatin remodeling Clinical consequences of mosaicism bear on both our ability to detect and make best decisions on behalf of our patients
4 Two Notions About Embryo Quality That from fertilization to Blast, the embryo dictates its developmental fate by expressing tangible/observable properties or byproducts reflecting implantation and term development potential Morphology/Morphokinetics/ omes /PGD- PGS/Mitochondria..amongst a cohort, those with potential can be differentiated from those lacking potetial That a zygote s developmental potential is determined prior to fertilization, that is inherent to gametes, and in no way manifests during the preimplantation window of development High quality gametes are few and far between and require pre-selection
5 Mosaicism noun mo sa ic \mō-ˈzā-ik\ a decoration on a surface made by pressing small pieces of colored glass or stone into a soft material that then hardens to make pictures or patterns the condition of possessing cells of two or more different genetic constitutions
6 Origins of chromosomal and non-chromosomal mosaicism are gametic and zygotic
7 A mitotic error that occurred in the trophectoderm of the blastocyst. The blastocyst is a mosaic; however, the error is isolated to the trophectoderm, while the inner cell mass remains euploid. Human Reproduction Update, Vol.20, No.4 pp , 2014 Advanced Access publication on March 25, 2014 doi: /humupd/dmu016
8 Opitz (again) Am J Med Genet Suppl. 1987;3: Western medicine is being sensitized to the enormous extent of prenatal death in humans at a time when such deaths, occurring after the first missed period, involve to an ever increasing degree wanted pregnancies conceived by women with rising mean maternal age, decreasing mean fertility, and ever greater desire and intention to assure a good pregnancy outcome. Available data suggest that about twothirds of human ova, embryos, and fetuses fail to reach birth or the end of the first year of life, with infant mortality of 1.06%, stillbirth rate of 8/1,000, abortion rate of about 15%, and death rate around the time of implantation estimated at 34%. Based on limited data on sperm, ova aspirated from Graafian follicles in infertile women, direct observation of a few implanting ova, the low rate of human fecundity, and the high failure rate of in vitro fertilization, it seems reasonable to suppose that about 30% of human ova perish at the time of fertilization and before implantation. Most of this prenatal death is attributable to chromosome abnormalities (aneuploidy and polyploidy), estimated to be present at the beginning of development in about half of all human ova or embryos.
9 Mosaicism is a common thing Metazoans rely on cell-cell variation and cope with
10 Mosaicism is the norm not the exception, as is developmental autonomy
11 Chromosomal abnormalities
12 Critical events during early mammalian development Get cell cycles in order- finish meiosis and start mitosis-major source of aneuploidies Erase maternal mrnas and stockpile maternal proteins (especially TFs for activating embryonic genome) Orient cell divisions to generate ICM and trophectoderm Equally distribute organelles (nucleoli, mitochondria, Golgi, centrosomes)
13 Gametic Contributions OOCYTE A haploid genome Mitochondria All of the organellar precursors to reconstruct 100 cells in a blastocyst 7 cell cycles worth of cyclins, tubulin (circa 64 mitotic spindles and cleavage furrows) SPERM A compacted haploid, non-functional genome desperately in need of a makeover A centrosome A spark (PLCzeta)
14 Good Gametes Make Good Embryos FROM HERE...TO...THERE Embryogenesis begins with Oogenesis Concept emerges that embryogenesis is about carving up the pie!
15 Blastocyst and inner cell mass Alessia Deglincerti, Gist Croft, and Ali H. Brivanlou
16 New look at mammalian embryos (Ellenberg, 2016) rev_ pdf
17 The tip of an iceberg: genetics Genetics is changing into a very non-mendelian thing Retains enormous diagnostic potential May avail molecular nanosurgery for corrective or eradicating lesions Is dominated presently by phase 3 technology gene editing Invading/reshaping practice of ARTs As are many other entrepreneurs with vivid imaginations and deep pockets to fill 17
18 Figure 1 Mechanisms of mosaicism involve perturbations in coordination between cell cycle, cytoskeleton, and chromatin remodeling Developmental Cell , DOI: ( /j.devcel ) Copyright 2016 Elsevier Inc. Terms and Conditions
19 Genomic instability starts with meiosis I and II in human oocytes
20 Mechanisms Underlying Genomic Instability weakened spindle checkpoint signaling supernumerary centrosomes defects in chromatid cohesion abnormal kinetochore-microtubule attachments increased spindle microtubule dynamics
21 Figure 2 Developmental Cell , DOI: ( /j.devcel ) Copyright 2016 Elsevier Inc. Terms and Conditions
22 Strange Cell Cycles Courtesy of Shu Hashimoto and Yoshi Morimoto Fertil Steril Jul;106(1): e6. doi: /j.fertnstert Multinucleation per se is not always sufficient as a marker of abnormality to decide against transferring human embryos.
23 Genomic instability is the norm not the exception
24 Clinical consequences of mosaicism bear on both our ability to detect and make best decisions on behalf of our patients
25 Am J Med Genet Feb;35(2): Incidence and timing of pregnancy losses: relevance to evaluating safety of early prenatal diagnosis. Simpson JL 1. Knowing the frequency and timing of pregnancy loss during normal gestation is integral to evaluating the safety of prenatal diagnostic techniques. That preclinical loss rates are high in humans has long been suspected, but in the past decade new data concerning these losses have become available. Cohort studies indicate that many women who show positive beta- HCG assays never show clinical evidence of pregnancy. Cytogenetic abnormalities have also recently been documented in 20% of ostensibly normal in vitro fertilization embryos. All the above are consistent with the sentinel studies of Hertig and Rock, who showed high frequencies of morphological abnormalities in preimplantation embryos. The imperfections of early human development The shortcomings of our technology
26 Aneuploidy is a bad thing
27 Mosaicism There is a selective advantage of the normal cell line, thus making it possible for a nonmosaic diploid fetus to result from an abnormal conception. It is possible to form a baby with entirely (or predominantly) normal cells from only a single diploid cell from the inner cell mass of the blastocyst (Lau et al., 1997; Robinson et al., 2002).
28 Blastomeres are not created equal!
29 Post-provocateuring. Preimplantation Diagnosis
30 Preimplantation diagnosis
31 DNA Microarray Reveals That High Proportions of Human Blastocysts from Women of Advanced Maternal Age Are Aneuploid and Mosaic high proportions of aneuploid blastocysts (69.2%) including aneuploid TE and euploid ICM, inconsistent anomalies between ICM and TE, or euploid TE cells and aneuploid ICM in the same blastocyst. Biopsy from TE in blastocysts does not exactly predict the chromosomal information in ICM if the embryos are aneuploid. Some mosaic blastocysts have euploid ICM% Liu et al. BIOLOGY OF REPRODUCTION (2012) 87(6):148, 1 9
32 Follow JARG for updates
33 Early influences
34 More than morphokinetics (Prof. Wolfe)
35 Greco et al., 2015 NEJM 35
36 Preimplantation Genetic Diagnosis - Aneuploidy In the absence of any fully euploid embryos, biopsies the transfer of mosaics, which may have appeared aneuploid using less sensitive methods, will sometimes result in a viable pregnancy. Munne, Grifo and Wells. Mosaicism: survival of the fittest versus no embryo left behind Fertility and Sterility
37 Percentages of mosaic, aneuploid and euploid embryos by age groups.
38 Munne et al.
39
40 embryo A2-A4 and D8-D11 Comparison of Lab Results Only Among 2/1110 (18.2%) embryos of embryos with demonstrated more than one within biopsy laboratory 5 (50%) congruent offered results between congruent both laboratory within lab evaluations. results. 4/11 (36.4%) All other of embryos, on repeat assessment demonstrated were varying found to outcomes be normal with 46, XX or different biopsy areas. 46, XY embryos.
41 Characteristics of Aneuploid embryos which implanted Patient N Embryos transferred PGS Result Outcome , XY, -13, -15, -18 Normal birth, 46, XY , XY, -21 Normal birth, 46, XY , XY, , XX Partial 47,XX,17p11.2-pter 45, XY, , XY, +22 Partial 45,XY,-1plar-p36,12 Normal birth, 46, XY Normal birth, 46, XX Normal birth 46, XY , XY, -21 Chemical pregnancy
42 Greco and Minasi, N Engl J Med 2015;373:
43 Very different from mouse and macaque New look at human embryos Nature Aug 24;537(7618): doi: /nature [Epub ahead of print] A developmental coordinate of pluripotency among mice, monkeys and humans. Nakamura T 1,2, Okamoto I 1,2, Sasaki K 1,2, Yabuta Y 1,2, Iwatani C 3, Tsuchiya H 3, Seita Y 3, Nakamura S 3, Yamamoto T 4,5,6, Saitou M 1,2,4,5.
44 Four cell mouse embryo contributes to different areas of the blastocyst Current Biology Volume 16, Issue 7, pr236 R239, 4 April 2006 Copyright 2006 Elsevier Ltd Terms and Conditions
45 Effects of preimplantation chromosome mosaicism on embryo development and survival Reversine-treated embryos formed blastocysts but failed to develop past implantation. Increasing the proportion of control blastomeres in the embryo rescued the lethal phenotype. Numbers represent the viability of early postimplantation embryos that had successfully implanted. Bolton et al. NATURE COMMUNICATIONS 7:11165 DOI: /ncomms
46 DNA Microarray Reveals That High Proportions of Human Blastocysts from Women of Advanced Maternal Age Are Aneuploid and Mosaic high proportions of aneuploid blastocysts (69.2%) including aneuploid TE and euploid ICM, inconsistent anomalies between ICM and TE, or euploid TE cells and aneuploid ICM in the same blastocyst. Biopsy from TE in blastocysts does not exactly predict the chromosomal information in ICM if the embryos are aneuploid. Some mosaic blastocysts have euploid ICM% Liu et al. BIOLOGY OF REPRODUCTION (2012) 87(6):148, 1 9
47 Summary Origins of mosaicism are both gametic and zygotic, influenced by age and ARTs Mechanisms of mosaicism involve perturbations during gametogenesis and early embryogenesis as a result of alterations in cell cycle checkpoints Clinical consequences of mosaicism are rooted in controversies as wide ranging as technicalities in detection and the likelihood that embryos that could have developed to term are instead being discarded
48 CHR Staff (* Visiting Scientists) David F Albertini, PhD David H Barad, MS, MD Ali Brivanlou, PhD, MD* Sarah Darmon, PhD, MS Norbert Gleicher, MD Vitaly A Kushnir, MD Emanuela Lazzaroni-Tealdi, MS Qi (Vicky) Wang, PhD Nico Santiquet, PhD Andrea Weghofer, PhD, MS, MBA, MD* Yan-Guang Wu, PhD* And our patients Affiliates University of Rochester School of Medicine and Dentistry: Aritro Sen, PhD Rockefeller University: Gist Croft, PhD Ali Brivanlou, PhD, MD Videos courtesy of Jean-Philippe Wolf Shu Hashimoto Yoshi Morimoto
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